In the 1760s, a round wooden temple appeared near Bolshaya Nevka in Staraya Derevnya. It was built at the expense of the statesman Alexei Petrovich Bestuzhev-Ryumin. However, in 1803, the church burned down when lightning struck it during a thunderstorm. Only the iconostasis was saved. The second stone temple with three chapels in the Empire style was built on the same place in 1805-1809. Architect V.O. Mochulsky supervised the construction of the new building.

Almost a hundred years later, in 1901, a sacristy and a bell tower were built next to the temple. The latter was demolished in 1947 during the construction of Primorsky prospect. During the Soviet period, a factory of rubber products was located in the Church of the Annunciation. By 1992, when the building was returned to the Orthodox Church, it was in critical condition. Restoration work started in 1999.

The exterior architectural decoration of the Annunciation Church is noteworthy. Its overall composition is designed in the style of classical manor churches, as they were created in the second half of the XVIII century. The yellow-painted building has the shape of a multi-tiered rotunda. Instead of the traditionally gilded drum there is a dome with a Tuscan colonnade.

In 2012, the bell tower reappeared as part of the temple complex which is actually a halved copy of the original one.